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Relationships between Müller cells and neurons in a primitive tetrapod, the Australian lungfish

Published online by Cambridge University Press:  02 June 2009

Stephen R. Robinson
Stephen R. Robinson
Affiliation:
Vision, Touch & Hearing Research Centre, University of Queensland, St. Lucia, QLD, Australia, 4072
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Abstract

We recently proposed a model of cytogenesis which assumes that primitive ancestral mammals and premammalian vertebrates had a retinal composition that consisted of about seven neurons per Müller cell, comprising 1–2 cone photoreceptors, 1–2 rod photoreceptors, 2–3 bipolar cells, 1–2 amacrine cells, less than 1 ganglion cell, and less than 1 horizontal cell (Reichenbach & Robinson, 1995). The Australian lungfish (Neoceratodus forsten) closely resembles the lobe-finned ancestors of land vertebrates, and has an extremely plesiomorphic nervous system. The present study, therefore, has examined the relative frequencies of retinal neurons and Müller cells (identified by immunolabelling for glutamine synthetase) in the lungfish retina. It was found that for each Müller cell there is an average of 1.9 cone photoreceptors, 1.7 rod photoreceptors, 3.1 amacrine/bipolar/horizontal cells, and 0.6 ganglion cells; amounting to a ratio of 7.3 neurons per Müller cell. These results support our conjecture that the sequence of cytogenesis in mammals is constrained by a developmental program that predates the evolution of mammals. The study also provides the first detailed morphological descriptions of lungfish Müller cells and their relationship with adjacent neurons. It was found that individual Müller cells in lungfish have a volume (more than 12,000 μm3) that is an order of magnitude higher than in mammals, yet the proportion of total retinal volume occupied by these cells (20%) is very similar.

Keywords

GliaGlutamateGlutamine synthetaseNeoceratodus forsteriPhotoreceptor
Type
Short Communications
Information
Visual Neuroscience , Volume 14 , Issue 4 , July 1997 , pp. 795 - 800
Copyright
Copyright © Cambridge University Press 1997

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References

Coates, M.I. & Clack, J.A. (1991). Fish-like gills and breathing in the earliest known tetrapod. Nature 352, 234–236.CrossRefGoogle Scholar
Dreher, Z., Robinson, S.R. & Distier, C. (1992). Müller cells in vascular and avascular retinae: A survey of seven mammals. Journal of Comparative Neurology 323, 59–80.CrossRefGoogle ScholarPubMed
Kemp, A. (1991). Australian Mesozoic and Camozoic lungfish. In Verte brate Palaeontology of Australasia, ed. Vickers-Rich, P., Monaghan, J.M., Baird, R.F. & Rich, T.H., pp. 465–496. Melbourne, Australia: Pioneer Design Studio.Google Scholar
Linser, P.J. (1991). Comparative immunocytochemistry of elasmobranch retina Muller cells and horizontal cells. Journal of Experimental Zoology (Suppl.) 5, 88–96.Google Scholar
Linser, P.J., Sorrentimg, M. & Moscona, A.A. (1984). Cellular compartmentalization of carbonic anhydrase-C and glutamine synthetase in developing and mature mouse neural retina. Developmental Brain Research 13, 65–73.CrossRefGoogle Scholar
Linser, P.J., Smith, K. & Angelides, K. (1985). A comparative analysis of glial and neuronal markers in the retina of fish: Variable character of horizontal cells. Journal of Comparative Neurology 237, 264–272.CrossRefGoogle ScholarPubMed
Locket, N.A. (1970). Landolt's club in the retina of the African lungfish. Protopterus aethiopicus. Heckel. Vision Research 10, 299–306CrossRefGoogle ScholarPubMed
Marshall, C.R. (1986). A list of fossil and extant Dipnoans. Journal of Morphology (Suppl.) 1, 15–24.CrossRefGoogle Scholar
Northcutt, R.G. (1986). Lungfish neural characters and their bearing on Sarcopterygian phylogeny. Journal of Morphology (Suppl.) 1, 277–297.CrossRefGoogle Scholar
Pow, D.V. (1994). Taurine, amino acid transmitters, and related molecules in the retina of the Australian lungfish Neoceratodus forsteri: A light microscopic immunocytochemical and electron-microscopic study. Cell and Tiissue Research 278, 311–326.CrossRefGoogle ScholarPubMed
Rasmussen, K.-E. (1975). A morphometric study of the Muller cell in rod and cone retinas with and uithout retinal vessels. Experimenial Eve Research 20, 151–166.CrossRefGoogle Scholar
Reichenbach, A., Hagen, E., Schippei, K. & Eberhardi, W. (1988). Quantitative electron microscopy of rabbit Muller (ghal) cells in dependence on retinal topography. Zeitschrift fur Mikroskopisch-Anatomische Forschung 102, 721–755.Google Scholar
Reichenbach, A., Schneider, H., Leibneiz, L., Reichell, P., Schaae, P., & Schumann, R., (1989). The structure of rabbit retinal Muller (ghal) cells is adapted to the surrounding retinal layers. Anatomy and Embryology 180, 71–79.CrossRefGoogle Scholar
Reichenbach, A. & Robinson, S.R. (1995). Phylogenetic constraints on retinal organisation and development. Progress in Retinal and Eye Research 15, 139–171.CrossRefGoogle Scholar
Robinson, S.R. (1991). Development of the mammalian retina. In Neuroanatomy of the Visual Pathways and Their Development, ed. Dreher, B. & Robinson, S.R., pp. 69–128. UK: Macmillan Press.Google Scholar
Robinson, S.R. (1994). Early vertebrate colour vision. Nature 367, 121.CrossRefGoogle Scholar
Robinson, S.R. (1996). A glimpse into the past: Müller cells in a primitive tetrapod. Journal for Brain Research 37, 226.Google Scholar
Robinson, S.R. & Dreher, Z. (1990). Müller cells in adult rabbit retinae: Morphology, distribution and implications for function and development. Journal of Comparative Neurology 292, 178–192.CrossRefGoogle ScholarPubMed
Sassoé Pognetto, M., Panzanelli, P., Atero, C., Fasolo, A. & Cantino, D. (1992). Comparative study of glial fibrillary acidic protein (GFAP)-like immunoreactivity in the retina of some representative vertebrates. European Journal of Histochemistry 36, 467–477.Google ScholarPubMed
Vaughan, D.K. & Lasater, E.M. (1990). Glial and neuronal markers in bass retinal horizontal and Müller cells. Brain Research 537, 131–140.CrossRefGoogle ScholarPubMed